|LIBBRECHT, ROMAIN - University Of Lausanne|
|WURM, YANNICK - University Of London|
|RIVA, OKSANA - University Of Lausanne|
|KELLER, LAURENT - University Of Lausanne|
Submitted to: PLoS Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/3/2013
Publication Date: 8/15/2013
Citation: Corona, M.V., Libbrecht, R., Wurm, Y., Riva, O., Keller, L. 2013. Vitellogenin Underwent Subfunctionalization to Acquire Caste and Behavioral Specific Expression in The Harvester Ant Pogonomyrmex barbatus. PLoS Genetics. doi: 10.1371/journal.pgen.1003730.
Interpretive Summary: Ants and bees, having evolved sociability independently, exhibit intriguing similarities and differences in their social organization. Vitellogenin (Vg), a yolk protein that in honey bees is involved in the regulation of division of labor, is a primary candidate to study whether notwithstanding their differences in sociality origin, the genetic pathways underlying division of labor are conserved between both groups. Contrasting with honey bees, which have a single Vg gene, we identified two Vg genes (Pb_Vg1 and Pb_Vg2) in the genome of the harvester ant P. barbatus. In order to investigate whether the occurrence of multiple Vg genes is extended to other species, we searched for Vg sequences in other ant genomes. We found that multiple Vg genes occur in several, but not all of the analyzed species. Combined phylogenetic and expression analyses revealed that, after the initial duplication in ants, Vg genes acquired caste and behavioral specific expression associated to reproduction and division of labor. Pb_Vg1 was highly expressed in queens compared to workers and in nurses compared to foragers, while Pb-Vg2 was preferentially expressed in foragers. Pb_Vg1 was the predominant transcript in queen and nurses, a pattern similar to that observed in honey bees. Overall, our results show that even though ants and bees evolved sociability independently, they have evolved similar mechanisms to regulate division of labor
Technical Abstract: Similarly to others advanced social insects, ants and bees have an age-associated division of labor, whereby young workers normally perform tasks inside the colony and old workers forage outside the nest, but this pattern is more variable in ants. It is unknown whether, notwithstanding their differences in sociality origin, the genetic pathways underlying division of labor are conserved between both groups. The reproductive ground plan hypothesis (RGPH) proposes that the physiological pathways regulating reproduction were co-opted to regulate worker behavior. In honey bees, support for this hypothesis is provided from studies demonstrating that the reproductive potential of workers, assessed by the levels of the yolk protein vitellogenin (Vg), is linked to task performance. Interestingly, contrary to honey bees that have a single Vg ortholog and nurses are potentially fertile, the genome of the harvester ant Pogonomyrmex barbatus harbors two Vg genes (Pb_Vg1-2) and nurses produce unfertile trophic eggs. P. barbatus, thus, provides a unique model to investigate whether Vg duplication in ant species was followed by subfunctionalization to acquire reproductive and non-reproductive nutritionally related functions and whether Vg reproductive function was co-opted to regulate worker behavior in sterile workers. To carry out these goals, we analyzed the phylogenetic relationships of Vg genes in Hymenoptera and compared the expression patterns of P. barbatus Vg genes among queens, nurses and foragers. Our result analysis revealed that, after the initial duplication in ants, Vg genes underwent neo-or subfunctionalization to acquire caste and behavioral specific functions. Pb_Vg1 was highly expressed in queens compared to workers and in nurses compared to foragers; while Pb_Vg2 was preferentially expressed in foragers. Pb_Vg1 was the predominant transcript in queen and nurses, a pattern similar to that observed in honey bees. Our results are both consistent with the RGPH and a nutritional regulation of division of labor.